Synergistic Effect of Plant-Growth-Promoting Rhizobacteria Improves Strawberry Growth and Flowering with Soil Salinization and Increased Atmospheric CO2 Levels and Temperature Conditions

Biofertilization with plant-growth-promoting rhizobacteria (PGPR) can positively affect the growth and health of host plants and reinforce their tolerance of stressors. Here, we investigate the use of isolated PGPR consortia from halophytes to improve strawberry growth and flowering performance under saline and elevated CO2 and temperature conditions. Growth, flower bud production, and the photosynthetic apparatus response were determined in strawberry plants grown at 0 and 85 mmol L−1 NaCl and in two atmospheric CO2-temperature combinations (400/700 ppm and 25/+4 °C, respectively). Biofertilization improved strawberry plant growth and flower bud production, independently of salinity conditions, at ambient CO2 and 25 °C, while bacterial inoculation only had a positive effect on plant growth in the presence of salt in high CO2 and at +4 °C. Biofertilizers 1 and 3 generated the largest biomass of strawberries at 400 ppm CO2 and 0 and 85 mmol L−1 NaCl, respectively, while biofertilizer 1 did so in the presence of salt and in an atmosphere enriched with CO2 and at +4 °C. The effect of the consortia was mediated by bacterial strain PGP properties, rather than by an improvement in the photosynthetic rate of the plants. Furthermore, biofertilizers 1 and 2 increased the number of flower buds in the absence of salt, while biofertilizers 3 and 4 did so for salt-inoculated plants at 400 ppm CO2 and at 25 °C. There was no effect of inoculation on flower bud production of plants grown at high CO2 and at +4 °C. Finally, we concluded that the effect of bacterial inoculation on strawberry growth and flowering depended on the type of bacterial strain and growth conditions. This highlights the importance of developing studies considering stress interaction to assess the real potential of biofertilizers.

[1]  P. Poczai,et al.  Evaluation of Plant Growth-Promoting and Salinity Ameliorating Potential of Halophilic Bacteria Isolated From Saline Soil , 2022, Frontiers in plant science.

[2]  R. Singh,et al.  Plant-soil-microbes: A tripartite interaction for nutrient acquisition and better plant growth for sustainable agricultural practices. , 2022, Environmental research.

[3]  Manish Kumar,et al.  Role of plant growth-promoting rhizobacteria in boosting the phytoremediation of stressed soils: Opportunities, challenges, and prospects. , 2022, Chemosphere.

[4]  Jennifer Mesa-Marín,et al.  Consortia of Plant-Growth-Promoting Rhizobacteria Isolated from Halophytes Improve the Response of Swiss Chard to Soil Salinization , 2022, Agronomy.

[5]  J. García-López,et al.  Consortia of Plant-Growth-Promoting Rhizobacteria Isolated from Halophytes Improve Response of Eight Crops to Soil Salinization and Climate Change Conditions , 2021, Agronomy.

[6]  L. Agrawal,et al.  Paenibacillus lentimorbus Enhanced Abiotic Stress Tolerance Through Lateral Root Formation and Phytohormone Regulation , 2021, Journal of Plant Growth Regulation.

[7]  L. Pecoraro,et al.  Plant Growth Promoting Rhizobacteria, Arbuscular Mycorrhizal Fungi and Their Synergistic Interactions to Counteract the Negative Effects of Saline Soil on Agriculture: Key Macromolecules and Mechanisms , 2021, Microorganisms.

[8]  Megha D. Bhatt,et al.  Molecular Mechanisms Deciphering Cross-Talk Between Quorum Sensing Genes and Major Iron Regulons in Rhizospheric Communities , 2021 .

[9]  E. Pajuelo,et al.  Impact of Plant Growth Promoting Bacteria on Salicornia ramosissima Ecophysiology and Heavy Metal Phytoremediation Capacity in Estuarine Soils , 2020, Frontiers in Microbiology.

[10]  Fan Yang,et al.  Increased contribution of root exudates to soil carbon input during grassland degradation , 2020, Soil Biology and Biochemistry.

[11]  E. M. Naranjo,et al.  Effect of Plant Growth-Promoting Rhizobacteria on Salicornia ramosissima Seed Germination under Salinity, CO2 and Temperature Stress , 2019, Agronomy.

[12]  Paulo Henrique Sales Guimarães,et al.  Beneficial effects of inoculation of growth-promoting bacteria in strawberry. , 2019, Microbiological research.

[13]  K. Kadirvelu,et al.  Plant growth promoting rhizobacteria (PGPR): A potential alternative tool for nematodes bio-control , 2019, Biocatalysis and Agricultural Biotechnology.

[14]  K. Dassanayake,et al.  Interaction of Elevated Carbon Dioxide and Temperature on Strawberry (Fragaria × ananassa) Growth and Fruit Yield , 2018 .

[15]  I. Caçador,et al.  Disentangling the effect of atmospheric CO2 enrichment on the halophyte Salicornia ramosissima J. Woods physiological performance under optimal and suboptimal saline conditions. , 2018, Plant physiology and biochemistry : PPB.

[16]  G. Beattie,et al.  Mining Halophytes for Plant Growth-Promoting Halotolerant Bacteria to Enhance the Salinity Tolerance of Non-halophytic Crops , 2018, Front. Microbiol..

[17]  J. Marques,et al.  Atmospheric CO2 enrichment effect on the Cu-tolerance of the C4 cordgrass Spartina densiflora. , 2018, Journal of plant physiology.

[18]  Li Xu,et al.  Integrated DNA methylome and transcriptome analysis reveals the ethylene-induced flowering pathway genes in pineapple , 2017, Scientific Reports.

[19]  N. Das,et al.  Application of Biofilms on Remediation of Pollutants - An Overview , 2017 .

[20]  K. Yamane,et al.  PGPR Improves Yield of Strawberry Species under Less-Fertilized Conditions , 2017 .

[21]  S. Ramakrishnan,et al.  Modeling the contributing factors of desertification and evaluating their relationships to the soil degradation process through geomatic techniques , 2015 .

[22]  P. Jardin Plant biostimulants: Definition, concept, main categories and regulation , 2015 .

[23]  A. Rizvi,et al.  Role of plant growth promoting rhizobacteria in sustainable production of vegetables: Current perspective , 2015 .

[24]  B. Glick,et al.  Bacterial Modulation of Plant Ethylene Levels , 2015, Plant Physiology.

[25]  Kemal Kazan,et al.  Diverse roles of jasmonates and ethylene in abiotic stress tolerance. , 2015, Trends in plant science.

[26]  M. Ashraf,et al.  The role of mycorrhizae and plant growth promoting rhizobacteria (PGPR) in improving crop productivity under stressful environments. , 2014, Biotechnology advances.

[27]  U. Pérez-López,et al.  Lettuce production and antioxidant capacity are differentially modified by salt stress and light intensity under ambient and elevated CO2. , 2013, Journal of plant physiology.

[28]  NeriDavide,et al.  Strawberry production in forced and protected culture in Europe as a response to climate change , 2012 .

[29]  Tingting Dong,et al.  Effects of Elevated CO2 and Temperature on Yield and Fruit Quality of Strawberry (Fragaria × ananassa Duch.) at Two Levels of Nitrogen Application , 2012, PloS one.

[30]  Vipin Kumar,et al.  Effect of GA3 and IAA on growth and flowering of carnation. , 2012 .

[31]  I. Kennedy,et al.  Importance of Biofilm Formation in Plant Growth Promoting Rhizobacterial Action , 2010 .

[32]  M. E. Figueroa,et al.  Salt stimulation of growth and photosynthesis in an extreme halophyte, Arthrocnemum macrostachyum. , 2010, Plant biology.

[33]  A. S. Raghavendra,et al.  The impact of global elevated CO2 concentration on photosynthesis and plant productivity , 2010 .

[34]  B. Lugtenberg,et al.  Plant-growth-promoting rhizobacteria. , 2009, Annual review of microbiology.

[35]  S. Ercişli,et al.  Does climate change have an effect on strawberry yi̇eld i̇n colder growi̇ng areas , 2009 .

[36]  Priyanka Sharma,et al.  Effects of 28-homobrassinolide on growth, lipid peroxidation and antioxidative enzyme activities in seedlings of Zea mays L. under salinity stress , 2008, Acta Physiologiae Plantarum.

[37]  R. Lada,et al.  Compensatory effects of elevated CO2 concentration on the inhibitory effects of high temperature and irradiance on photosynthetic gas exchange in carrots , 2007, Photosynthetica.

[38]  T. Luque,et al.  Growth and photosynthetic responses to salinity of the salt-marsh shrub Atriplex portulacoides. , 2007, Annals of botany.

[39]  D. Van Der Straeten,et al.  The plant stress hormone ethylene controls floral transition via DELLA-dependent regulation of floral meristem-identity genes , 2007, Proceedings of the National Academy of Sciences.

[40]  S. Schiavon,et al.  Climate Change 2007: Impacts, Adaptation and Vulnerability. , 2007 .

[41]  J. Castillo,et al.  Growth and photosynthetic responses to salinity in an extreme halophyte, Sarcocornia fruticosa , 2006 .

[42]  Jun Huang,et al.  Immobilization of Pycnoporus sanguineus laccase on copper tetra‐aminophthalocyanine–Fe3O4 nanoparticle composite , 2006, Biotechnology and applied biochemistry.

[43]  E. Aloni,et al.  Role of cytokinin and auxin in shaping root architecture: regulating vascular differentiation, lateral root initiation, root apical dominance and root gravitropism. , 2006, Annals of botany.

[44]  T. Sharkey,et al.  Diffusive and metabolic limitations to photosynthesis under drought and salinity in C(3) plants. , 2004, Plant biology.

[45]  K Maxwell,et al.  Chlorophyll fluorescence--a practical guide. , 2000, Journal of experimental botany.

[46]  M. Sánchez-Díaz,et al.  Effects of Temporary Droughts on Photosynthesis of Alfalfa Plants , 1993 .

[47]  E. Brugnoli,et al.  Effects of Salinity on Stomatal Conductance, Photosynthetic Capacity, and Carbon Isotope Discrimination of Salt-Tolerant (Gossypium hirsutum L.) and Salt-Sensitive (Phaseolus vulgaris L.) C(3) Non-Halophytes. , 1991, Plant physiology.

[48]  I. Ohad,et al.  Membrane protein damage and repair: removal and replacement of inactivated 32-kilodalton polypeptides in chloroplast membranes , 1984, The Journal of cell biology.